The Himalayan uplift and evolution of aquatic biodiversity across Asia: Snowtrout (Cyprininae: Schizothorax) as a test case

RESEARCH ARTICLE The Himalayan uplift and evolution of aquatic biodiversity across Asia: Snowtrout (Cyprininae: Schizothorax) as a test case Binod Regmi1¤, Marlis R. Douglas1, Karma Wangchuk1,2, Zachery D. Zbinden1, David R. Edds3, Singye Tshering2, Michael E. DouglasID1* 1 Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, United States of America, 2 National Research & Development Centre for Riverine and Lake Fisheries, Ministry of Agriculture & Forests, Royal Government of Bhutan, Thimphu, Bhutan, 3 Department of Biological Sciences, Emporia State University, Emporia, Kansas, United States of America ¤ Current address: National Institute for Arthritis, Musculoskeletal & Skin Diseases (NIAMS), National Institute of Health, Bethesda, Maryland, United States of America * med1@uark.edu Abstract Global biodiversity hotspots are often remote, tectonically active areas undergoing climatic fluctuations, such as the Himalaya Mountains and neighboring Qinghai-Tibetan Plateau (QTP). They provide biogeographic templates upon which endemic biodiversity can be mapped to infer diversification scenarios. Yet, this process can be somewhat opaque for the Himalaya, given substantial data gaps separating eastern and western regions. To help clar- ify, we evaluated phylogeographic and phylogenetic hypotheses for a widespread fish (Snowtrout: Cyprininae; Schizothorax) by sequencing 1,140 base pair of mtDNA cyto- chrome-b (cytb) from Central Himalaya samples (Nepal: N = 53; Bhutan: N = 19), aug-

mented with 68 GenBank sequences (N = 60 Schizothorax/N = 8 outgroups). Genealogical relationships (N = 132) were analyzed via maximum likelihood (ML), Bayesian (BA), and haplotype network clustering, with clade divergence estimated via TIMETREE. Snowtrout seemingly originated in Central Asia, dispersed across the QTP, then into Bhutan via south- ward-flowing tributaries of the east-flowing Yarlung-Tsangpo River (YLTR). Headwaters of five large Asian rivers provided dispersal corridors from Central into eastern/southeastern Asia. South of the Himalaya, the YLTR transitions into the Brahmaputra River, facilitating successive westward colonization of Himalayan drainages first in Bhutan, then Nepal, fol- lowed by far-western drainages subsequently captured by the (now) westward-flowing Indus River. Two distinct Bhutanese phylogenetic groups were recovered: Bhutan-1 (with three subclades) seemingly represents southward dispersal from the QTP; Bhutan-2 appar- ently illustrates northward colonization from the Lower Brahmaputra. The close phyloge- netic/phylogeographic relationships between the Indus River (Pakistan) and western tributaries of the Upper Ganges (India/Nepal) potentially implicate an historic, now disjunct connection. Greater species-divergences occurred across rather than within-basins, sug- gesting vicariance as a driver. The Himalaya is a component of the Earth’s largest glacial reservoir (i.e., the “third-pole”) separate from the Arctic/Antarctic. Its unique aquatic PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0289736 October 24, 2023 1 / 27

a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Regmi B, Douglas MR, Wangchuk K, Zbinden ZD, Edds DR, Tshering S, et al. (2023) The Himalayan uplift and evolution of aquatic biodiversity across Asia: Snowtrout (Cyprininae: Schizothorax) as a test case. PLoS ONE 18(10): e0289736. https://doi.org/10.1371/journal. pone.0289736 Editor: Tzen-Yuh Chiang, National Cheng Kung University, TAIWAN Received: September 5, 2022 Accepted: July 26, 2023 Published: October 24, 2023 Copyright: © 2023 Regmi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data available via Genbank repository: Haplotype GenBank Accession Number 58thun003 OR373078 58DAKP06 OR373079 58BERT01 OR373080 58khar001 OR373081 58pots002 OR373082 58puza001 OR373083 58thun008 OR373084 58danr004 OR373085 58NYAC01 OR373086 58haac001 OR373087 58DAKP011 OR373088 58DIKC03 OR373089 58KAME01 OR373090 58shen006 OR373091 58TOEB12 OR373092 58danr001